Prominent bacterial heterotrophy and sources of
[superscript 13]C-depleted fatty acids to the interior
Canada Basin
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Citation
Shah, S. R., D. R. Griffith, V. Galy, A. P. McNichol, and T. I.
Eglinton. “Prominent bacterial heterotrophy and sources of 13Cdepleted fatty acids to the interior Canada Basin.”
Biogeosciences 10, no. 11 (November 7, 2013): 7065-7080.
As Published
http://dx.doi.org/10.5194/bg-10-7065-2013
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Final published version
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Wed May 25 18:50:20 EDT 2016
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http://hdl.handle.net/1721.1/82929
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Biogeosciences
Open Access
Biogeosciences, 10, 7065–7080, 2013
www.biogeosciences.net/10/7065/2013/
doi:10.5194/bg-10-7065-2013
© Author(s) 2013. CC Attribution 3.0 License.
Prominent bacterial heterotrophy and sources of 13C-depleted fatty
acids to the interior Canada Basin
S. R. Shah1 , D. R. Griffith2 , V. Galy3 , A. P. McNichol1 , and T. I. Eglinton4
1 Geology
and Geophysics Department, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole,
MA 02543, USA
2 MIT/WHOI Joint Program in Oceanography, 266 Woods Hole Rd., Woods Hole, MA 02543, USA
3 Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods
Hole, MA 02543, USA
4 Swiss Federal Institute of Technology, Zurich, Switzerland
Correspondence to: S. R. Shah (sshah@whoi.edu)
Received: 28 March 2013 – Published in Biogeosciences Discuss.: 11 April 2013
Revised: 25 September 2013 – Accepted: 8 October 2013 – Published: 7 November 2013
Abstract. In recent decades, the Canada Basin of the Arctic
Ocean has experienced rapidly decreasing summer sea ice
coverage and freshening of surface waters. It is unclear how
these changes translate to deeper waters, particularly as our
baseline understanding of organic carbon cycling in the deep
basin is quite limited. In this study, we describe full-depth
profiles of the abundance, distribution and carbon isotopic
composition of fatty acids from suspended particulate matter at a seasonally ice-free station and a semi-permanently
ice-covered station. Fatty acids, along with suspended particulate organic carbon (POC), are more concentrated and
13 C-enriched under ice cover than in ice-free waters. But
this influence, apparent at 50 m depth, does not propagate
downward below 150 m depth, likely due to the weak biological pump in the central Canada Basin. Branched fatty acids
have δ 13 C values that are similar to suspended POC at all
depths and are more 13 C-enriched than even-numbered saturated fatty acids at depths above 3000 m. These are likely
to be produced in situ by heterotrophic bacteria incorporating organic carbon that is isotopically similar to total suspended POC. Below surface waters, there is also the suggestion of a source of saturated even-numbered fatty acids which
could represent contributions from laterally advected organic
carbon and/or from chemoautotrophic bacteria. At 3000 m
depth and below, a greater relative abundance of long-chain
(C20−24 ), branched and unsaturated fatty acids is consistent
with a stronger influence of re-suspended sedimentary organic carbon. At these deep depths, two individual fatty acids
(C12 and iso-C17 ) are significantly depleted in 13 C, allowing
for the possibility that methane oxidizing bacteria contribute
fatty acids, either directly to suspended particulate matter or
to shallow sediments that are subsequently mobilized and incorporated into suspended particulate matter within the deep
basin.
1
Introduction
In the past two decades, the Arctic Ocean’s Canada Basin
has seen both rapidly decreasing summer sea ice coverage
(Maslanik et al., 2011; McLaughlin et al., 2011; Stroeve et
al., 2007) and freshening of surface waters (Macdonald et al.,
2002; McPhee et al., 2009; Yamamoto-Kawai et al., 2009).
These changes have been accompanied by a deepening of the
chlorophyll maximum depth (Jackson et al., 2010; McLaughlin and Carmack, 2010), and a trend towards smaller phytoplankton cell sizes and increased bacterial abundance in surface waters (Li et al., 2009). Combined with the observed
decrease in primary productivity in the increasingly ice-free
Canada Basin (Cai et al., 2010; Grebmeier et al., 2010; Lee et
al., 2012), these trends will likely result in decreasing export
of organic carbon to the deep basin and sediments.
Across ocean basins, sinking particulate organic carbon
(POC) flux has been shown to correlate with bacterial abundance and productivity at deeper depths (Nagata et al., 2010;
Yokokawa et al., 2013). Prior to the recent decline in summer
Published by Copernicus Publications on behalf of the European Geosciences Union.
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
Biogeosciences, 10, 7065–7080, 2013
170˚W
130˚W
140˚W
150˚W
160˚W
120˚W
˚N
Rid
74
72
˚N
N
78˚
ge
−
r th
wi
nd
sea ice, ice-tethered sediment traps in the Canada Basin
documented a much smaller POC flux through the upper
200 m than is observed in other oligotrophic regions (Honjo
et al., 2010). Despite a vanishingly small, and likely decreasing supply of autochthonous organic carbon exported
from the sea surface, prokaryotic abundance at mesopelagic
and bathypelagic depths in the Canada Basin (> 100 m) were
found to be comparable to subtropical and equatorial regions
(He et al., 2012; Uchimiya et al., 2013). This imbalance between prokaryotic abundance and sinking POC flux suggests
the importance of an alternate carbon and energy source supporting microbial productivity in the deep Canada Basin.
Heterotrophic bacterial productivity at mesopelagic depths
could be supported by labile organic carbon produced by
phytoplankton in the productive Chukchi Sea and laterally
supplied as dissolved organic carbon (DOC) at mesopelagic
depths (Davis and Benner, 2007; Mathis et al., 2007; Shen et
al., 2012; Walsh et al., 1989). Long-distance lateral transport
of re-suspended sedimentary particles has also been observed
below 100 m depth (Honjo et al., 2010; Hwang et al., 2008;
Jackson et al., 2010; O’Brien et al., 2013), delivering associated organic carbon to the interior Canada Basin. In addition
to bacterial heterotrophy, significant bathypelagic chemoautotrophy is suggested by the radiocarbon and stable isotopic
composition of dissolved inorganic carbon (DIC), sinking
POC and suspended POC (Griffith et al., 2012). The dynamics between prokaryotic production and organic carbon cycling appears to be distinct from other oligotrophic ocean
basins and the questions of what carbon and energy sources
support bacterial production in the dark Canada Basin and
how they change with time will be highly relevant to predicting the future of organic carbon sequestration and cycling in
this deep Arctic Basin.
To advance our understanding of organic carbon cycling in
Canada Basin, we investigated the distribution and isotopic
composition of fatty acids from suspended POC collected
at two deep-basin stations in 2008, a summer with recordlow sea ice coverage (Maslanik et al., 2011). Isotopic studies of bulk organic carbon pools have addressed the supply
and fate of vertically and laterally delivered organic carbon
to the interior Canada Basin (Griffith et al., 2012; Honjo et
al., 2010; Hwang et al., 2008). The provenance and cycling of
organic matter are better understood in the Mackenzie River
and Beaufort shelf and slope because DOC and POC analyses have been complemented by isotopic studies of fatty
acids and other biomarkers (Drenzek et al., 2007; Goñi et
al., 2005; Tolosa et al., 2013). Fatty acids are integral components of bacterial and eukaryotic membranes. They can
therefore derive both from microbial cells suspended at depth
and from degraded organic carbon associated with sinking
particles or re-suspended sediments when recovered from
suspended POC. Although multiple sources are represented,
isotopic analysis of fatty acids allows for more specific investigations of microbial processes which are difficult to resolve
through bulk analyses. Here we present the results of our in-
No
7066
CB9
Au
g
200
8
CHUKCHI
SEA
76˚N
Sea
Ice
Exte
nt
CB4
74˚N
CANADA BASIN
70
˚N
72˚N
0
50
−3
00
−25
50
68˚
−1
N
BEAUFORT
SEA
0
0
0
−5
MACKENZIE
RIVER
160˚W
150˚W
140˚W
70˚N
68˚N
130˚W
Fig. 1. Sampling locations in the Canada Basin mapped with approximate sea-ice extent in August 2008 (http://nsidc.org/data/).
vestigations and discuss the multiple organic carbon sources
and bacterial metabolic strategies that could contribute to the
observed profiles.
2
2.1
Material and methods
Sampling
Suspended particulate matter was collected during the Joint
Ocean Ice Study (JOIS) in 2008 from two stations in the
Canada Basin of the Arctic Ocean: CB4 (seasonally icefree; 74◦ 59.99800 N; 150◦ 0.00200 W; 3825 m bottom depth)
and CB9 (semi-permanently ice-covered; 77◦ 59.85900 N;
150◦ 4.88700 W; 3821 m bottom depth), illustrated in Fig. 1.
At both stations, McLane WTS-LV pumps filtered particulate material onto pre-combusted 142 mm glass fiber filters
(Whatman GF/F; 0.7 µm) in situ after being lowered to specific depths. A more detailed description of sample collection
is provided by Griffith et al. (2012). Filters were packaged
into envelopes of pre-combusted aluminium foil, frozen at
−20 ◦ C, and were subsequently partitioned for radiocarbon
analysis (Griffith et al., 2012) and for lipid analysis. Samples
destined for lipid extraction were maintained at −20 ◦ C for
three years until processing.
2.2
Lipid extraction, identification and quantification
Total lipids were extracted from frozen filters in 50 mL
of methylene chloride/methanol (9 : 1), assisted by the Microwave Accelerated Reaction System (MARS Xpress, CEM
Corp) at 100 ◦ C for 20 min. The filter extraction procedure
was repeated with fresh solvents and both extracts were combined, passed through a 0.45 µm PTFE filter and evaporated
to dryness under a stream of ultra-high purity N2 . Combined extracts were saponified in 1 mL of 0.2 M KOH in
methanol/water (4 : 1) at 80 ◦ C for 2 h. Neutral lipids were
www.biogeosciences.net/10/7065/2013/
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
2.3
Isotopic analysis of FAMEs
Compound-specific δ 13 C analysis of FAMEs was performed
at the Organic Mass Spectrometry Facility at the Woods Hole
Oceanographic Institution (WHOI) on an HP-6890 GC coupled to a Finnigan-MAT DeltaPlus IRMS. FAME samples
were injected using a Gerstel CIS-4 programmable temperature vaporizing (PTV) injector, separated on a Varian CPSil5CB column, and the GC was interfaced using a FinniganMAT GC Combustion Interface III (modified with an integral
fused silica combustion system at 860 ◦ C). GC-IRMS measurements were made in triplicate and uncertainty is reported
as the larger of the standard deviation of three measurements
or analytical uncertainty (0.3 ‰). Overall system accuracy
and precision were confirmed to be better than 0.3 ‰ based
on a suite of nine externally analyzed standards. Measured
δ 13 C values of FAMEs are expressed relative to the PDB
standard and corrected for addition of the methyl carbon
during trans-esterification by mass balance (Supplement Table 1). Values reported in Table 2 are also corrected for fatty
acids contributed by organic carbon adsorption. The adsorption blank was defined by the abundance and isotopic composition of fatty acids from the blank filter (Tables 1 and 2).
www.biogeosciences.net/10/7065/2013/
Σ FA (ng/L)
1
10 100 1000
B
Relative Abundance of Fatty Acids
0%
50%
100%
12:0
50 m
50 m
13:0
150 m
150 m
14:0
1000 m
15:0
2000 m
i-15:0
1000 m
2000 m
2500 m
3000 m
Station CB4
Station CB4
A
2500 m
3000 m
3500 m
3500 m
3750 m
3750 m
ai-15:0
16:0
Σ16:1
i-16:0
17:0
50 m
150 m
500 m
1000 m
Station CB9
i-17:0
Station CB9
recovered by three extractions with hexane after addition of
10 % NaCl. The pH of the remaining aqueous layer was lowered to ∼ 1 by dropwise addition of 6 N HCl, and the acid
fraction was recovered by three additional extractions with
hexane/methylene chloride (4 : 1). The distribution of total
lipids in 10 % subsamples of neutral and acid fractions were
determined by GC-TOF as trimethylsilyl ether derivatives.
The remaining 90 % of acid fractions were transesterified to
convert fatty acids into their methyl esters by refluxing in 5 %
HCl in MeOH (with known δ 13 C value) at 70 ◦ C for 12 h. After adding MilliQ water to cooled vials, fatty acid methyl esters (FAMEs) were recovered by extracting three times with
hexane/methylene chloride (9 : 1). Extracts were dried with
sodium sulfate and concentrated under a stream of ultrahigh purity N2 . FAMEs from trans-esterified acid fractions
were identified by comparison of retention times with a 37component FAME mixture (Supelco part number 47885-U)
and bacterial FAMEs mixture (Matreya part number 1114),
and for a few representative samples, by GC-MS. Quantification of FAMEs was performed by GC-FID with an external calibration curve and assigned a conservative 5 % uncertainty. The contribution of fatty acids from the sorption of
organic carbon to the GF/F filter was subsequently corrected
for by subtraction of surface-area-normalized abundances recovered from a 142 mm GF/F filter lowered to 3805 m water
depth but not pumped through (Table 1).
7067
50 m
150 m
500 m
1000 m
18:0
Σ18:1
20:0
22:0
24:0
Fig. 2. (a) Summed concentration of total fatty acids. (b) Relative
abundances of individual fatty acids with blue shades representing even-numbered fatty acids and orange shades representing oddnumbered and branched fatty acids and purple shades representing
long-chain fatty acids.
3
3.1
Results
Bulk analysis of suspended POC
The concentration and isotopic composition of suspended
POC was described by Griffith et al. (2012) and exhibits similar profiles at both stations. At near-surface depths, the semipermanently ice-covered station (CB9) has a higher concentration of suspended POC than the seasonally ice-free station
(CB4). Despite similar radiocarbon ages, CB9 is also more
13 C-enriched at 9 and 50 m depth. But at deeper depths, suspended POC concentrations converge on similar, very low
values (≤ 0.04 µM) with δ 13 C values of −25 to −23 ‰ (Griffith et al., 2012). The sorption of dissolved organic carbon
onto glass fiber filters during their time immersed in seawater was also investigated. A 142 mm GF/F filter lowered
to 3805 m water depth, but not pumped through, yielded
3.1 µmol of organic carbon from half of the filter area with
a δ 13 C value of −25.1 ‰ (Griffith et al., 2012). The distribution of fatty acids recovered from the other half of the blank
filter and their δ 13 C values are described in Tables 1 and 2
and discussed below.
3.2
Concentration of fatty acids
Analysis of fatty acids was performed on separate fractions
of the same filters used for suspended POC measurements.
As with POC, fatty acid concentrations decrease with depth
(Fig. 2a). Below 1500 m, the sill depth of the Canada Basin,
fatty acid abundances at CB4 are < 10 ng L−1 . Despite these
low abundances, the concentration of fatty acids recovered
from the blank filter was less than fatty acids from filtered
seawater at all depths (Table 1).
Although both POC and fatty acid concentrations are
higher (per liter seawater) under ice cover than in open
Biogeosciences, 10, 7065–7080, 2013
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
7068
Table 1. Concentration of POC and FAMEs in the Canada Basin.
Seasonally ice-free station CB4
Depth (m)
Volume Filtered (L)
50
207
150
828
1000
901
DOC blank
(ng/filter)
2000
950
2500
924
Ice-covered station CB9
3000
901
3500
931
3750
912
50
188
(ng L−1 seawater)
150
46
500
906
1000
917
(ng L−1 seawater)
74954
10081
2390
828
558
338
485
498
478
15853
n.d.∗
1528
993
2116
406.88
60.27
20.01
8.34
7.80
2.17
2.93
1.93
559.01
180.15
16.15
15.20
12:0
13:0
14:0
15:0
16:0
17:0
18:0
20:0
22:0
24:0
51
0
100
26
906
17
891
24
0
0
0.00
0.00
125.09
4.68
206.35
0.73
46.91
0.00
2.24
0.96
1.50
0.26
9.72
1.69
25.19
0.55
16.38
0.00
0.10
0.18
0.38
0.05
1.62
0.51
7.34
0.19
7.67
0.00
0.00
0.18
0.00
0.00
0.11
0.10
3.07
0.07
4.36
0.05
0.03
0.00
0.00
0.00
0.18
0.07
3.30
0.04
3.74
0.03
0.03
0.03
0.02
0.02
0.32
0.09
0.68
0.01
0.47
0.02
0.01
0.07
0.08
0.01
0.35
0.10
1.05
0.03
0.70
0.03
0.02
0.07
0.02
0.00
0.19
0.07
0.83
0.02
0.31
0.01
0.00
0.08
1.47
0.00
128.85
6.57
271.53
1.87
67.60
1.68
0.00
3.53
0.08
0.00
5.04
1.02
59.56
0.61
108.51
1.18
0.21
0.00
0.01
0.04
2.35
0.44
7.53
0.20
3.43
0.00
0.10
0.00
0.00
0.00
0.43
0.20
5.66
0.14
7.61
0.00
0.04
0.00
SFA
POC
Total FA
2015
386.98
55.57
17.93
7.79
7.42
1.71
2.44
1.53
483.10
176.22
14.09
14.10
i-15:0
ai-15:0
i-16:0
i-17:0
ai-17:0
0
0
0
0
0
6.40
4.66
0.52
0.52
0.00
1.72
1.30
0.35
0.32
0.00
0.70
0.75
0.22
0.18
0.00
0.10
0.13
0.03
0.06
0.00
0.08
0.08
0.02
0.04
0.00
0.09
0.10
0.02
0.04
0.00
0.09
0.09
0.03
0.03
0.00
0.10
0.08
0.03
0.04
0.00
9.73
4.54
0.00
1.10
0.00
0.75
0.60
0.26
0.29
0.00
0.62
0.51
0.18
0.16
0.00
0.25
0.28
0.11
0.12
0.00
BFA
0
12.10
3.69
1.85
0.32
0.22
0.25
0.23
0.25
15.37
1.89
1.46
0.75
616 : 1
618 : 1
0
47
0.94
1.98
0.14
0.28
0.02
0.06
0.01
0.00
0.01
0.01
0.07
0.05
0.05
0.04
0.04
0.01
31.94
14.04
0.35
0.13
0.05
0.14
0.04
0.05
MUFA
47
2.92
0.42
0.08
0.01
0.02
0.12
0.09
0.05
45.98
0.48
0.19
0.09
18:2n6
18:3n6
20:2
0
0
54
1.49
3.39
0.00
0.41
0.19
0.00
0.00
0.15
0.00
0.05
0.07
0.11
0.00
0.14
0.01
0.00
0.08
0.00
0.02
0.11
0.03
0.00
0.08
0.02
5.22
9.34
0.00
0.38
0.49
0.70
0.13
0.28
0.00
0.10
0.16
0.00
PUFA
54
4.88
0.60
0.15
0.23
0.15
0.08
0.16
0.09
14.56
1.57
0.41
0.26
∗ n.d. not determined
Table 2. Blank-corrected δ 13 C values of POC and FAMEs in the Canada Basin.
DOC blank
Seasonally ice-free station CB4
50 m
(‰)
(‰)
±
POC
−25.1
0.1
12:0
14:0
15:0
16:0
17:0
18:0
SFA
−27.9
−30.0
1.0
0.3
−26.5
0.4
−36.2
−34.0
−36.0
0.7
0.7
0.3
−25.9
−26.4
0.3
2.3
−30.4
−35.4
i-15:0
ai-15:0
i-17:0
BFA
±
1000 m
(‰)
±
−24.8
0.1
−22.7
0.1
0.5
3.1
−29.6
−30.1
−25.7
−29.7
−28.5
−28.8
−29.7
0.3
0.5
0.3
0.3
0.5
0.3
2.6
−27.4
−23.6
−22.7
−26.0
−23.3
−28.4
−27.0
0.4
0.5
1.1
0.5
1.0
0.3
2.3
−31.2
−28.4
0.5
0.3
−24.6
−24.1
0.5
0.3
−30.0
2.6
−24.4
2.0
−21.8
−22.7
−21.0
−22.1
0.5
0.3
0.9
1.8
−29.5
0.1
150 m
(‰)
±
2000 m
(‰)
±
−23.0
0.1
2500 m
(‰)
±
−22.7
0.1
−20.4
−22.4
−27.2
−23.7
−27.8
−27.6
0.6
1.1
0.4
1.0
0.3
2.4
−25.5
−24.8
−28.1
0.3
0.6
0.4
−27.7
−27.8
0.3
2.4
−21.7
−22.7
0.8
0.5
−23.1
−22.6
0.7
1.3
−22.3
1.6
−22.8
1.3
Ice-covered station CB9
3000 m
(‰)
±
3500 m
(‰)
±
3750 m
(‰)
±
−24.5
0.1
−24.3
0.1
−24.6
0.1
−42.9
−25.1
−26.2
−22.9
−23.1
−22.2
−23.8
2.6
0.3
0.6
0.3
0.6
0.6
1.9
−32.0
−25.3
−25.7
−24.5
−23.0
−22.8
−24.7
0.9
0.4
0.3
0.3
0.8
0.3
2.1
−37.7
−25.0
−28.3
−25.8
−23.8
−29.8
−27.2
0.6
0.3
0.5
0.4
0.6
0.3
2.3
−24.4
−23.8
−41.8
−27.4
0.9
0.6
2.8
1.6
−25.1
−24.6
−39.8
−27.3
0.5
0.3
0.3
2.3
−22.7
−22.7
−22.1
−22.6
0.5
0.6
0.9
1.6
16:1n9
18:1n9
MUFA
18:2n6
1POC−SFA
1POC−BFA
1SFA−BFA
1.3
5.8
0.5
−5.3
4.9
−0.4
−5.3
4.3
−0.6
−4.9
4.7
−0.7
−5.4
5.1
0.1
−5.0
−0.7
2.9
3.6
0.3
3.0
2.6
2.6
−2.0
−4.6
50 m
(‰)
±
150 m
(‰)
±
−27.0
0.1
n.d.
−34.5
−30.8
−35.2
0.4
0.4
0.3
−27.9
0.3
−29.1
0.6
−29.8
−34.2
0.7
3.0
−29.1
−29.1
0.3
2.5
−26.3
−24.7
0.4
0.3
−25.8
2.2
−28.6
−32.7
−29.9
0.3
0.4
2.7
−26.5
0.9
7.2
−1.2
−8.4
500 m
(‰)
±
1000 m
(‰)
±
−24.1
0.1
n.d.
−26.9
−25.4
−28.0
−25.2
−28.7
−27.9
0.4
0.4
0.4
0.7
0.3
2.4
−24.8
−22.3
−27.3
1.3
0.9
0.4
−28.6
−27.9
0.3
2.4
−23.9
−22.9
−23.0
−23.4
0.3
0.3
0.3
2.0
−22.6
−22.0
1.5
0.3
−22.3
1.4
3.7
−0.7
−4.5
−5.6
∗ n.d. not determined
Biogeosciences, 10, 7065–7080, 2013
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S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
Normalized FA Concentrations
Depth (m)
(ng/µg POC)
0 1 2 3 10 20 30
0
//
Station CB9 (ice-covered)
B
(ng/µg POC)
0 1 2 3 10 20 30
//
0
40
1000
1000
2000
2000
3000
3000
4000
//
Normalized FA Concentrations
4000
A
//
B
Station CB4 (ice-free)
Station CB9 (ice-covered)
δ 13 C (‰)
13
δ C (‰)
40
-45
0
Depth (m)
Station CB4 (ice-free)
A
7069
SFA
MUFA
PUFA
BFA
1000
2000
-40
-35
-30
-25
-45
-20
-40
-35
-30
-25
-20
0
12:0
14:0
i-15:0
ai-15:0
15:0
16:0
i-17:0
17:0
18:0
POC
DOC
1000
2000
3000
3000
4000
4000
14:0
i-15:0
ai-15:0
15:0
16:1n9
16:0
i-17:0
17:0
18:2n6
18:1n9
18:0
POC
DOC
Fig. 3. POC-normalized concentrations of fatty acids grouped into
saturated (SFA), branched (BFA), monounsaturated (MUFA) and
polyunsaturated (PUFA) and plotted with depth at (a) Station CB4
and (b) Station CB9.
Fig. 4. δ 13 C values of individual fatty acids with depth where SFAs
are in blue shades, BFAs are in orange shades and open circles represent MUFAs and PUFAs for (a) Station CB4 and (b) Station CB9.
POC and DOC (Griffith et al., 2012) are represented by black lines.
water (Fig. 2a), fatty acids account for a greater fraction
of suspended particulate organic carbon at station CB4
compared to CB9 at 50 m (Fig. 3a). POC-normalized fatty
acids also reveal a subsurface enrichment of saturated, evennumbered fatty acids at 2500 m depth (Fig. 3a). This peak
results from disproportionately low suspended POC concentrations combined with fatty acid concentrations on par with
the sample from 2000 m (Table 1). At mesopelagic depths,
between 150 and 1000 m, a more modest enrichment in POCnormalized bacterial branched fatty acids was revealed at station CB4 (Fig. 3). These subsurface enrichments are superimposed on a general decreasing trend of POC-normalized
fatty acids with depth. Similar POC-normalized values were
observed in the shallow profile from CB9 (Fig. 3b). In the
abyssal Canada Basin, however, very low POC-normalized
concentrations were found which did not decrease with
depth, suggesting a different composition or source of suspended POC in the deepest 1000 m (Fig. 3a).
a distinction between the distribution of fatty acids found
above 3000 m, and those found at and below this depth. In
the deepest 1000 m, saturated C16 and C18 continue to be
the most abundant fatty acids although C14 is relatively more
abundant than above. We also observe greater proportions of
MUFAs and branched fatty acids (BFAs), as well as longchain C20−24 fatty acids, supporting a distinct source of suspended POC at these depths.
3.3
Distribution of fatty acids
At 50 m depth, the most abundant lipids at both stations were
saturated C14 and C16 fatty acids (Fig. 2b). Monounsaturated
(MUFAs) and polyunsaturated fatty acids (PUFAs) are only
significant contributors to total fatty acids at station CB9
at 50 m depth. Appreciable concentrations of PUFAs were
not recovered from either station. Below 50 m, C16 and C18
fatty acids make up the majority of total fatty acids, followed
by iso- and anteiso-C15 at both stations. There is a general
pattern of decreasing relative C14 abundance and increasing
C18 abundance with depth, and a proportionally important
contribution from C15 fatty acids in the shallowest 1000 m
(Fig. 2a). A similar pattern of relative abundances is observed
at station CB9, although with two important exceptions: the
C18 -dominated sample at 150 m where C18 also drives the
larger concentration of total fatty acids found at CB9 compared to the same depth at CB4, and more abundant unsaturated fatty acids at 50 m. At station CB4, Fig. 2b illustrates
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3.4
Isotopic composition of fatty acids
At both stations in the Canada Basin, all individual fatty acids
from 50 m depth are depleted in 13 C compared to the same
lipids recovered from deeper depths (Fig. 4a and b). Saturated C14 , C15 and C16 fatty acids display the largest δ 13 C
deviations (e.g., 6–13 ‰ for C16 fatty acid), while others are
more modestly depleted. A similar pattern can be observed
in suspended POC from the near-surface depths compared
to below (δ 13 C deviation of 3–6 ‰; (Griffith et al., 2012).
In all samples, odd-numbered and branched fatty acids (orange shades in Fig. 4) are generally enriched in 13 C compared to even-numbered fatty acids (blue shades in Fig. 4).
The abundance-weighted average δ 13 C values of BFAs are
within 1 ‰ of POC above 3000 m depth at station CB4 while
the SFAs are depleted in 13 C by 4.3–5.8 ‰ (Table 2). This
pattern is also reflected in an average 5 ‰ enrichment of
BFAs compared to saturated fatty acids (SFAs) between 50
and 2500 m. δ 13 C values from station CB9 hint at a similar pattern although sampling limitations resulted in fewer
possible comparisons. At 3000 m and below, there is a shift
towards 13 C-enriched SFAs such that the δ 13 C values of
SFAs more closely match suspended POC than the δ 13 C
values of BFAs do (Table 2). The exceptions to this pattern are the C12 and iso-C17 fatty acids. C12 fatty acids are
depleted by 7–19 ‰ compared to average SFA values despite
being within 1 ‰ higher in the water column. Uncorrected
δ 13 C values of C12 fatty acid are within analytical uncertainty between 3000 and 3750 m (Supplement Table 1), but
Biogeosciences, 10, 7065–7080, 2013
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S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
isotopic variability emerged from mass-balance blank corrections (Fig. 4a). While it is possible that this variability is
an artefact of our blank determination method, the C12 fatty
acid is unambiguously 13 C-depleted compared to the rest of
the water column in the abyssal Canada Basin. Branched
iso-C17 fatty acids are also very depleted in 13 C at 3000 m
and below. Its δ 13 C values are more negative at 3000 and
3500 m than any fatty acid observed higher in the water column (Fig. 4a).
4
Discussion
The profile of fatty acids at stations CB4 and CB9 show
strong similarities with open-ocean settings although concentrations are much smaller. Saturated C14 and C16 fatty
acids are the most abundant fatty acids in the epipelagic waters of the Canada Basin (Fig. 2b) as well as other coastal and
open-ocean regions (Gutiérrez et al., 2012; Hamanaka et al.,
2002; Loh et al., 2008; Schultz and Quinn, 1972; Tolosa et
al., 2004, 2013; Wakeham, 1995; Wakeham et al., 2010; Xu
and Jaffé, 2007). In many shallow locations, unsaturated fatty
acids follow C14 and C16 in abundance, but these are scarce
at 50 m in the Canada Basin as they were in a high Arctic fjord during the summer months (Mayzaud et al., 2013).
However, the absence of unsaturated fatty acids could also result from their degradation during sample storage or extraction and may not reflect the true distribution of fatty acids
in the Canada Basin. We therefore interpret the absence of
unsaturated fatty acids with caution, particularly as PUFAs
were detected in suspended POC collected from the moreproductive coastal areas of the Beaufort Sea (Connelly et
al., 2012; Tolosa et al., 2013). At deeper depths, the dominance of saturated C16 and C18 fatty acids mirrors other oligotrophic water columns (Loh et al., 2008; Wakeham, 1995).
Although we noted a greater concentration of total fatty
acids under ice cover than in open water (Fig. 2a), this
contrast is small compared to the difference between the
Canada Basin and much-higher concentrations observed in
low-latitude epipelagic regions (e.g., Hamanaka et al., 2002;
Tolosa et al., 2004; Wakeham, 1995; Wakeham et al., 2010).
But the overall decreasing trend of POC-normalized fatty
acids above 3000 m (Fig. 3), also seen in the oligotrophic
central Pacific and Sargasso Sea (Loh et al., 2008; Wakeham, 1995), suggests fatty acids in the Canada Basin behave
similarly to low-latitude oligotrophic oceans where they are
thought to be among the more labile components of POC.
The concentration and isotopic composition of fatty acids
in suspended POC from the Canada Basin reflect vertically
stratified organic carbon sources at surface depths, in the interior basin, and in the deepest 1000 m. In the following sections, we discuss the possible origin of fatty acids found on
the blank filter as well as the phytoplanktonic, microbial, and
advected sources of fatty acids to the stratified layers of the
Canada Basin.
Biogeosciences, 10, 7065–7080, 2013
4.1
Sources of the organic carbon sorption blank
The sorption of DOC onto glass fiber filters is a widely recognized contributor of non-particulate organic carbon to suspended POC samples collected by in situ pumps (Gardner
et al., 2003; Moran et al., 1999; Schultz and Quinn, 1973).
As pumps are lowered into the water, filters likely accumulate this organic carbon near the surface where the highest
concentrations of DOC, suspended POC and bacterial abundance are found. The sampling depth, at which the filter
has the longest soaking time, is also a possible contributor
to the sorption blank. At station CB4, the radiocarbon content of adsorbed organic carbon measured on a filter that
traveled the length of the water column and was held at
3805 m depth while POC from other depths were sampled
(−247 ± 9 ‰) is very similar to DOC at 20 m water depth
(−234 ± 5 ‰) (Griffith et al., 2012) while the δ 13 C value of
adsorbed organic carbon (−25.1 ± 0.1 ‰, Table 2) is intermediate between the δ 13 C values of DOC (−22.1 ± 0.1 ‰)
(Griffith et al., 2012) and suspended POC (−29.5 ± 0.1 ‰,
Table 2) at the surface. Interestingly, the 114 C and δ 13 C
values from the blank filter are also similar to suspended POC at 3000 m and below (114 C = −227 ± 40 ‰,
δ 13 C = −24.6 ± 0.1 ‰ at 3750 m; Griffith et al., 2012). We
calculate the possible contributions of these sources following the dual isotope mass balance approach outlined by Griffith et al. (2012). These calculations indicate 27 % of the
sorbed organic carbon blank could derive from surface DOC
(114 C = −234 ± 5 ‰, δ 13 C = −22.1 ± 0.1 ‰ at 20 m), 35 %
surface POC (114 C = +8 ± 9 ‰, δ 13 C = −29.5 ± 0.1 ‰
at 50 m), and 38 % deep DOC (114 C = −494 ± 2 ‰,
δ 13 C = −23.1 ± 0.1 ‰ at 3807 m), assigning the majority of
organic matter sorption to surface waters.
Fatty acids found in the adsorption blank do not resemble suspended POC in shallow waters, however, either in
their distribution or isotopic composition. C16 and C18 fatty
acids dominate, as they do in suspended POC from 150 m
and below (Fig. 2b). Although fatty acids point toward a
deeper source region for adsorbed organic carbon than bulk
isotopic considerations do, it is possible that this discrepancy can be explained if adsorbed organic carbon preferentially incorporates attached bacterial biomass rather than
total organic carbon in surface waters or if it incorporates
bacterial biomass from 3805 m depth with a fatty acid distribution that echoes that found at bacteria-dominated mesoand bathypelagic depths. The weighted average δ 13 C value
of fatty acids from the adsorption blank is similar to the
δ 13 C value of suspended POC (Table 2), following the pattern observed in BFAs from suspended POC between 150
and 2500 m, consistent with a heterotrophic bacterial source
(see Sect. 4.4). The 114 C value of the adsorption blank limits the contribution of surface-ocean bacteria incorporating
phytoplankton-derived organic carbon with the 114 C value
of DIC (+31 ± 4 ‰ at 20 m; Griffith et al., 2012), but not
bacteria incorporating “aged” DOC which would have the
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S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
same isotopic composition as the DOC sorption component
of the blank. Bacterial cells that attach to the blank filter at
bathypelagic depths would also contribute an “aged” 114 C
value to the adsorption blank. Although the depth at which
bacteria attach to glass fiber filters is ambiguous, we can assume that a contribution of fatty acids from non-particulate
sources is present at all depths. Taking our seawater-soaked
filter to be representative of this blank, we correct for their
contributions by subtraction (Table 1) or mass balance (Table 2).
4.2
Semi-permanently ice-covered vs. seasonally
ice-free surface waters
Previous work indicates that ice cover affects POC flux, bacterial abundance and bacterial productivity in the western
Arctic Ocean, but these investigations often combine the influences of ice cover and seasonality (Honjo et al., 2010;
Sherr and Sherr, 2003; Sherr et al., 2003) or compare the
shallower, nutrient-rich and more ice-free Chukchi Sea with
the western Canada Basin (He et al., 2012; Honjo et al., 2010;
Moran et al., 2005; Rich et al., 1998). We find supporting
evidence that ice cover affects the concentration and composition of epipelagic organic carbon within Canada Basin by
comparing stations CB4 and CB9. At the time of our sampling, station CB9, which was ice-covered, hosted a greater
concentration of suspended POC at 9 and 50 m depth which
was more 13 C-enriched compared to ice-free station CB4 (3–
6 ‰; Griffith et al., 2012). This contrast is unlike DIC and
DOC which have δ 13 C values within 0.5 ‰ between stations
at 20–25 m depth (Griffith et al., 2012).
The concentration and distribution of fatty acids also exhibit differences between the ice-covered and open-water
stations and offer clues to their cause. As with suspended
POC, the absolute abundance of total fatty acids is greater
and individual fatty acids are more 13 C-enriched under ice
cover (CB9) compared to open water (CB4; Figs. 2a and 4).
However, normalizing fatty acid concentrations to suspended
POC reveals the opposite pattern (Fig. 3), indicating that the
composition of suspended POC is different at the two stations. MUFAs and PUFAs are also only significant contributors to total fatty acids at station CB9 (Fig. 3). While SFAs
have more negative δ 13 C values than BFAs at both stations,
the isotopic contrast is much greater at station CB9 (8.4 ‰)
than CB4 (5.3 ‰; Table 2). Combined, these differences suggest different dynamics between bacterial and other components of POC at the two stations.
It has been reported that before the recent decline in summer sea ice in the Canada Basin, ice algae contributed up
to 57 % of total primary productivity and released a large
fraction (31–65 %) of the resulting organic matter as DOC
(Gosselin et al., 1998). This labile organic carbon is likely to
be enriched in 13 C compared to organic carbon produced by
phytoplankton in the water column (Belt et al., 2008; Forest
et al., 2007). The relative 13 C-enrichment of BFAs at station
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7071
CB9 compared to station CB4 (Fig. 4) could therefore reflect
greater bacterial dependence on organic carbon derived from
sea-ice algae because strong isotopic similarity is expected
between fatty acids produced by bacterial heterotrophs and
their organic carbon source (Blair et al., 1985; Hayes, 2001;
Monson and Hayes, 1982). At station CB9, the average δ 13 C
value of BFAs falls between suspended POC (−27.0 ‰) and
DOC (−21.7 ‰; Griffith et al., 2012) supporting greater bacterial incorporation of DOC under ice cover compared to station CB4 where the average BFA δ 13 C value is more negative
and very similar to suspended POC (Table 2). It does not appear that SFAs at 50 m have a 13 C-enriched, ice-algal source
at either station. Instead they are likely derived from phytoplankton in the water column.
During a late summer expedition in 2008, differences in
the vertical structure of phytoplankton and bacterial abundances were observed between CB4 and CB9 (He et al.,
2012) although comparable bacterial abundances were found
at our sampling depth of 50 m. This was the chlorophyll maximum depth during our sampling and it represented a maximum in both bacterial and phytoplankton abundance at station CB4 (He et al., 2012). However at station CB9, a larger
concentration of bacteria was found closer to the sea surface (He et al., 2012). The larger isotopic contrast between
SFAs and BFAs at station CB9 could thus be a result of
a spatial decoupling between primary production and heterotrophic production. The focusing of organic carbon production near the sea surface under greater sea ice coverage
(Gosselin et al., 1998) suggests that DOC released from ice
algae could fuel bacterial secondary production throughout
the upper 50 m under ice cover, while phytoplankton production at the chlorophyll maximum depth directly supports
bacterial production in open water. It is also possible that the
∼ 2 ‰ enrichment in both suspended POC and SFAs at station CB9 is a reflection of larger overall contributions from
heterotrophic bacteria compared to station CB4.
4.3
Sequestration of 13 C-depleted fatty acids in surface
waters
Suspended POC and individual fatty acids are significantly
depleted in 13 C in the near-surface compared to the water
column below (Fig. 4) while DIC and DOC are not (Griffith
et al., 2012). This could be explained by an allochthonous
source of 13 C-depleted particulate carbon, such as terrestrial material exported by the Mackenzie River. Although
neither station is proximal to a source of terrestrial organic
carbon, isotopic and elemental evidence indicates a substantial fraction of riverine fresh water becomes stored in
the surface layer of the central basin in some recent years
(Guay et al., 2009; Macdonald et al., 2002; YamamotoKawai et al., 2009). It has also been shown that surface-water
bacterioplankton can access and re-mineralize the presumably refractory terrestrial DOC delivered with it (Hansell
et al., 2004). However, the summer halocline particle trap
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S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
(Jackson et al., 2010) may isolate this influence from our
50 m samples, as these samples were collected below the
halocline in the Pacific Summer Water (PSW) layer (Griffith
et al., 2012). Isotopic evidence for proportionally greater terrestrial contributions to DOC in the surface layer in 2008 is
also lacking at both stations because the δ 13 C values of DOC
are similar throughout the upper 350 m (Griffith et al., 2012).
In addition, a δ 13 C transition from “light” terrestrial values
to a more 13 C-enriched marine primary source has been documented in sedimentary organic carbon much closer to shore
at the base of the Beaufort slope (Naidu et al., 2000).
An alternative explanation for “light” suspended POC and
fatty acids at 50 m depth is a large effective fractionation
factor between DIC and phytoplankton biomass. This depth
coincides with the chlorophyll maximum at both stations,
which a previous study found to be dominated by diatoms
(Gosselin et al., 1998). At this light-limited depth, most
13 C-depleted fatty acids (C , C
14
15 and C16 ) could be produced by slowly growing marine diatoms expressing their
maximum expected fractionation between 12 C and 13 C (Popp
et al., 1998), combined with an additional isotopic effect on
the large end of that observed between algal biomass and
fatty acids (Schouten et al., 1998). The “heavier” fatty acids
(e.g., iso-C15 , anteiso-C15 and C18 ) are likely to have greater
contributions from heterotrophic bacteria. Two of these, isoC15 , anteiso-C15 , have a known bacterial source (Kaneda,
1991). The isotopic similarity between bacterial fatty acids
and suspended POC (at station CB4) or between bacterial
fatty acids and a combination of DOC and POC (station CB9)
is consistent with bacterial heterotrophs incorporating organic carbon from POC and DOC (Blair et al., 1985; Hayes,
2001; Monson and Hayes, 1982).
The strong isotopic contrasts between 50 m and below
(Fig. 4) seem to indicate a weak coupling between surface
waters and the basin interior, caused by the ineffective biological pump that operates in the Canada Basin. The flux
of organic carbon through the shallowest 200 m is orders of
magnitude smaller than that found in other ocean basins, and
this small flux is accompanied by similarly minuscule fluxes
of diatom frustules and coccoliths (Honjo et al., 2010). Conditions and productivity at the sea surface do not appear to
have a controlling influence on suspended POC and fatty
acids at depth in the Canada Basin and the effects of sea ice
coverage discussed above are confined to surface waters, also
suggesting that seasonal influences may not strongly affect
the deep basin. Not only are the concentration and isotopic
composition of suspended POC very similar below 150 m
at stations CB4 and CB9 (Griffith et al., 2012), but a more
extensive survey of suspended POC concentrations below
100 m has revealed a general absence of gradients in the interior Canada Basin (Jackson et al., 2010). Bacterial abundances are also similar below 50 m near stations CB4 and
CB9 (He et al., 2012; Uchimiya et al., 2013). No significant
differences can be observed in fatty acids recovered from
both stations at 1000 m, either. Major differences do exist in
Biogeosciences, 10, 7065–7080, 2013
the abundance and distribution of fatty acids at 150 m depth,
but it is more likely that this sample represents an external influence such as POC delivered by a mesoscale eddy because
fatty acids are both unlike station CB4 at 150 m (Fig. 2a) and
unlike fatty acids above and below at station CB9 (e.g., small
relative concentrations of C14 , iso-C15 and anteiso-C15 fatty
acids compared to 50 and 1000 m). Such eddies have been
documented at approximately 150 m depth at locations more
proximal to the Northwind Ridge (Fig. 1), and are known
to transport nutrient- and organic carbon-rich Pacific-origin
seawater to the western Canada Basin (Mathis et al., 2007;
Pickart, 2004).
4.4
Bacterial heterotrophy in the interior Canada Basin
(150–2500 m)
Multiple features in the concentrations and δ 13 C values of
fatty acids indicate that heterotrophic bacteria suspended in
the water column are important contributors compared to
other sources of fatty acids in the interior Canada Basin. The
broad subsurface peak in the POC-normalized abundance of
BFAs in the shallowest 1000 m at station CB4 (Fig. 3a) may
be produced by a relatively large proportion of productive
bacterial heterotrophs synthesizing branched fatty acids at
mesopelagic depths where Honjo et al. (2010) have proposed
intense bacterial heterotrophy contributes to the weak biological pump. The isotopic divergence between BFAs and
even-numbered SFAs (∼ 5 ‰, Table 2) is, arguably, the most
consistent pattern in fatty acids above 3000 m depth and another indication of strong bacterial heterotrophy. Such divergent δ 13 C values between BFAs and other fatty acids are
not reported in suspended POC from surface waters of the
Mediterranean (Tolosa et al., 2004), near-surface, oxic depths
of the Black Sea (Wakeham et al., 2007) or near-surface, oxic
depths of the Cariaco Basin (Wakeham et al., 2010). Instead,
δ 13 C values of fatty acids and suspended POC in the interior Canada Basin evoke the isotopic relationship observed
in sinking particulate matter (Tolosa et al., 2004), as well
as net-heterotrophic riverine (Zou et al., 2006) and estuarine (Boschker et al., 2005) settings where external input of
terrestrial organic carbon supports bacterial secondary production. Unlike turbid estuaries and rivers, the Canada Basin
is particle-poor (Griffith et al., 2012), but a significant external, and possibly episodic source of laterally transported
organic carbon from the productive Chukchi Sea (Davis and
Benner, 2007; Mathis et al., 2007; Shen et al., 2012; Walsh
et al., 1989) or from re-suspended Beaufort Slope sediments
(Honjo et al., 2010; Hwang et al., 2008; Jackson et al., 2010;
O’Brien et al., 2013) has been shown.
The close isotopic relationship between BFAs and suspended POC (< 1 ‰ except 50 m at CB9, Table 2) at each individual depth above 3000 m is also striking (Fig. 4). Because
of the small expected isotopic fractionation between bacterial
heterotrophs and substrate organic carbon (Blair et al., 1985;
Monson and Hayes, 1982), this relationship indicates BFAs
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S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
are produced in situ by heterotrophic bacteria suspended in
the meso- and bathypelagic Canada Basin. Bacterial incorporation of DOC can not be ruled out between the depths of
500 and 2500 m, however, due to the close isotopic similarity
between POC and DOC (Fig. 4a; Griffith et al., 2012). Oddnumbered SFAs are also isotopically more similar to average
BFAs than average SFAs below 150 m, suggesting that a significant fraction of straight-chain C15 and C17 fatty acids are
produced by heterotrophic bacteria.
4.5
Sources of 13 C-depleted fatty acids in the interior
Canada Basin (150–2500 m)
The Canada Basin is vertically stratified, and the influence
of the Pacific-origin, Atlantic-origin and isolated deep basin
waters can be seen in the isotopic composition of DIC, DOC
and suspended POC (Griffith et al., 2012). The vertical distribution and δ 13 C values of fatty acids, however, do not appear
to be strongly influenced by water mass except for the possibility of Pacific-origin Summer Water (PSW), from which
the 50 m samples were obtained (Griffith et al., 2012). Instead, fatty acid distributions and isotopic compositions suggest three distinct zones in the water column: 50 m, 150–
2500 m, and 3000–3775 m.
Here we discuss the largest region, 150–2500 m, where a
13 C-depleted source of SFAs is suggested by the subsurface
peak in the POC-normalized abundance of SFAs at 2500 m
depth (Fig. 3a), 95 % of which is made up of C16 and C18
fatty acids (Fig. 2b). C16 fatty acid shows a progressive 13 Cdepletion between 500 and 2500 m depth, opposite to the
trend expected from decreasing contributions from surfacederived, “light” organic matter and increasing relative contributions from “heavy” bacterial heterotrophs. The δ 13 C value
of saturated C18 fatty acid also remains similar to its value at
50 m rather than trending towards a more positive value with
depth as would be consistent with an increasingly important
bacterial heterotrophic source. Near these depths, the possibility of significant microbial DIC incorporation was suggested by an isotopic mixing model of radiocarbon and δ 13 C
values of bulk carbon pools (Griffith et al., 2012) pointing towards a third, chemoautotrophic source of fatty acids in the
interior Canada Basin.
We identify four sources of organic matter that may contribute to the total fatty acids that we recovered between
150 and 2500 m: (1) phytoplankton-derived organic carbon
produced in surface waters; (2) laterally delivered organic
carbon originating either from primary productivity in the
Chukchi Sea or from re-suspended shelf sediments; (3) suspended bacterial cells with unspecified metabolism; and (4)
non-particulate organic carbon adsorbed onto the glass fiber
filters during sample collection. We have explicitly corrected
for adsorbed organic carbon (Tables 1 and 2) and only consider the first three fatty acid sources in the following model
and discussion.
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7073
In order to explore the potential importance of the three
fatty acid sources to the interior Canada Basin, we construct
an isotopic mass balance model according to
1 = fsurface + fadvected + fbacteria
(1)
δmeasured = fsurface · δsurface + fadvected · δadvected
+ fbacteria · δbacteria ,
(2)
where δ represents δ 13 C value. We focus on 1000–2500 m
where the isotopic divergence between SFAs and BFAs is
most pronounced at station CB4 (Fig. 4a). We also consider
only C16 and C18 fatty acids, which represent 84–95 % of
total fatty acids at these depths (Table 1).
δsurface : although the sinking flux of organic carbon is
known to be very small (Honjo et al., 2010), and the 13 Cdepleted isotopic signature of fatty acids in surface waters
does not appear to form the major component of fatty acids
in suspended POC below 50 m depth (Fig. 4), surface-derived
organic matter delivered with sinking particles will still contribute some fraction of fatty acids to the interior Canada
Basin. We assign δsurface as the average δ 13 C value of C14 and
C16 at 50 m at station CB4. Because the δ 13 C value of C18 is
more similar to BFAs than SFAs, it likely represents greater
contributions from heterotrophic bacteria and is therefore not
included in our endmember value for phytoplankton-derived
organic matter. Although 50 m may appear deep for a surface
source, we believe our 50 m samples, taken at the chlorophyll
maximum, to be a reasonable proxy for the isotopic composition of sinking fatty acids. The mechanisms of organic matter
aggregation and the depths from which it is dominantly exported are not well-understood in the central Canada Basin,
but the sequestration of nutrients below the summer halocline
means that a large proportion of total water column primary
productivity occurs at the subsurface chlorophyll maximum
depth (Lee et al., 2012; Martin et al., 2012). A recent analysis of suspended particulate matter from the coastal Beaufort Sea also identifies a POC maximum and biomarker indications of “fresh” organic carbon at the chlorophyll maximum depth (Tolosa et al., 2013). This is unlike lower-latitude
ocean basins where the subsurface chlorophyll maximum
does not correspond to a biomass or productivity maximum.
δadvected : the δ 13 C values and distribution of fatty acids
from allochthonous organic carbon in the interior Canada
Basin are much more difficult to assign because of multiple
and poorly defined possible sources. Organic carbon from
primary productivity over the Chukchi (Davis and Benner,
2005, 2007; Shen et al., 2012) or Beaufort shelves (OrtegaRetuerta et al., 2012) could be incorporated into suspended
POC following deposition to sediments, re-suspension and
lateral transport (Mathis et al., 2007). Saturated C14 , C16
and C18 fatty acids in sediments at the base of the Beaufort
slope, presumably with a Beaufort Sea primary origin, have
more enriched δ 13 C values relative to those between 150 and
Biogeosciences, 10, 7065–7080, 2013
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
2500 m (Drenzek et al., 2007; Goñi et al., 2005). Sea-ice algae will also contribute organic carbon that is 13 C-enriched
(Belt et al., 2008; Budge et al., 2008). Bioavailable DOC with
undefined δ 13 C value may also be incorporated directly into
suspended POC by aggregation processes (Burd and Jackson, 2009; Engel et al., 2004). We use δ 13 C values from ice
algal, phytoplankton and copepod fatty acids reported from
samples collected near Barrow, Alaska (Budge et al., 2008)
to represent δadvected values for fresh and re-worked sources
of organic carbon from nearby productive waters (Table 3).
Beaufort shelf sediments also host organic matter delivered by the Mackenzie River (Drenzek et al., 2007; Goñi
et al., 2005; Yunker et al., 2005), and their mobilization
could deliver marine, terrestrial and riverine organic carbon
to the interior Canada Basin. We also use the δ 13 C value of
fatty acids from Mackenzie River suspended POC (Goñi et
al., 2005; Tolosa et al., 2013) and Beaufort slope sediments
(Drenzek et al., 2007; Goñi et al., 2005; Tolosa et al., 2013)
to represent δadvected values for sedimentary fatty acids (Table 3).
fbacteria : because the δ 13 C value of bacterial fatty acids
will depend on an unknown fraction of bacterial heterotrophs
vs. chemoautotrophs and on chemoautotrophic pathways, we
allow δbacteria to be an unknown variable and instead estimate fbacteria from prokaryotic abundances and a biomassto-phospholipid fatty acid conversion factor assuming phospholipid fatty acids are the major source of fatty acids in marine bacteria (Oliver and Colwell, 1973; Oliver and Stringer,
1984). Using prokaryotic abundances reported by Uchimiya
et al. (2013), the carbon content of bacterial cells in oligotrophic waters (4–7 fg C cell−1 ; Christian and Karl, 1994;
Gundersen et al., 2002), and considering that 49 % of microbial cells pass through GF/F filters (Lee et al., 1995), we
calculate that 11–14 % of suspended POC captured in our
samples could be attributed to prokaryotic biomass carbon
between 1000 and 2500 m depth (Fig. 5). Although δ 13 C
values of BFAs indicate that at least some of this prokaryotic biomass is heterotrophic bacteria (Sect. 4.4), this range
falls within the 10–22 % of suspended POC that Griffith et
al. (2012) attribute to chemoautotrophic biomass based on
the radiocarbon similarity between DIC and suspended POC
and the modest 13 C enrichment in POC between 1000 and
2500 m. Total prokaryotic biomass reported by Uchimiya et
al. (2013) includes both bacterial and archaeal cells while
only bacterial cells will be represented in fatty acid abundances. Still, there appears to be a relatively constant offset
between the fraction of POC from total prokaryotic biomass
and from fatty acid carbon (Fig. 5) which supports suspended prokaryotes as a dominant source of fatty acids at
these depths. In their intact phospholipid form, fatty acids are
thought to be a constant fraction of bacterial biomass (Balkwill et al., 1988; Findlay et al., 1989; White et al., 1979).
The ratio of fatty acid carbon to biomass carbon is poorly
constrained for slowly growing deep ocean bacterioplankton,
but for a sedimentary enrichment culture with large bacterial
Biogeosciences, 10, 7065–7080, 2013
Fraction of POC
0%
10%
20%
30%
0
500
1000
Depth (m)
7074
1500
2000
2500
3000
3500
prokaryotic
biomass C
fatty acid C
4000
Fig. 5. Proportions of total POC that can be attributed to prokaryotic biomass and organic carbon from fatty acids (FA). Prokaryotic
organic carbon calculated from abundances reported by Uchimiya
et al. (2013) with a conversion factor of 6.5 ± 2.5 fg carbon cell−1
(Christian and Karl, 1994; Gundersen et al., 2002) and assuming
51 % recovery on GF/F filters (Lee et al., 1995). Fatty acid abundances converted organic carbon equivalents using the weighted average % C for fatty acids at each depth.
cells (56 fg C cell−1 ), 21 % of biomass carbon could be attributed to fatty acid carbon from phospholipids (Findlay et
al., 1989). It has also been observed that approximately half
of total phospholipid is lost upon transitioning a marine bacterium from nutrient-replete culture conditions to suspension
in seawater (Oliver and Stringer, 1984), so on this basis we
assume fatty acid carbon is approximately 10 % of biomass
carbon. An additional assumption about the proportional balance between bacterial and archaeal cells must be made to
calculate fbacteria . A dominance of bacteria was reported below 500 m at the base of the Chukchi Slope (Kirchman et
al., 2007), however this dominance would yield more bacterial fatty acid than we recovered from all depths between
500 and 2500 m. The maximum proportion of bacteria that
fatty acid abundances allow is 54 %, closer to the fraction of
bacteria found at meso- and bathypelagic depths of the oligotrophic North Pacific and Atlantic Oceans (Herndl et al.,
2005; Karner et al., 2001). Conservatively, we assume that
50 % of prokaryotic cells are bacterial and that 10 % of their
biomass carbon can be attributed to fatty acid carbon. Using
an abundance-weighted fatty acid composition to calculate
fatty acid carbon from observed fatty acid abundance, these
assumptions yield an fbacteria value that averages 80 % between 1000 and 2500 m.
www.biogeosciences.net/10/7065/2013/
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
7075
Table 3. δ 13 C values of organic matter sources that could be laterally supplied to Canada Basin.
Representative
δadvected (‰)
Ice Algae
Phytoplankton
−24.0
−30.6
Copepod
Beaufort Slope Sediments
−27.4
−27.0
Mackenzie River POC
−35.0
Reference
avg. C16:4 δ 13 C values; Budge et al. (2008)
avg. C16:0 , C16:1 , C16:4 , C18:0 , C18:1 δ 13 C values;
Budge et al. (2008), chlorophyll maximum from Tolosa et al. (2013)
avg. C16:4 δ 13 C values; Budge et al. (2008)
avg. C16:0 , C16:1 , C18:0 δ 13 C values; Goñi et al. (2005),
Drenzek et al. (2007); slope sites from Tolosa et al. (2013)
avg. C14:0 , C16:0 , C16:1 δ 13 C values; Goñi et al. (2005),
Mackenzie River site from Tolosa et al. (2013)
Defining δmeasured as the average δ 13 C value for C16 and
C18 fatty acids between 1000 and 2500 m depth (−27.5 ‰),
three unknown variables remain: fsurface , fadvected and
δbacteria . Combining equations (1) and (2) to eliminate fsurface
leaves:
0.10
0.05
0.00
60%
Macken
-26.0
(3)
relating fadvected to δbacteria by a linear equation in the form
y = mx + b. Figure 6 illustrates the relationship between
fadvected and δbacteria for the full range of possible fadvected
values (0–20 %). Considering that fadvected + fsurface = 20 %,
this corresponds to fsurface values of 20 % to 0 % (Fig. 6, secondary horizontal axis). Each line in Fig. 6 represents a solution to the mass balance equation for a different advected
component (summarized in Table 3).
Bacterial heterotrophs will likely synthesize fatty acids
with δ 13 C values similar to BFAs and POC at each depth
(Sect. 4.4): −21 to −23 ‰ between 1000 and 2500 m. Model
results, however, are uniformly more negative than these values implying production of 13 C-depleted fatty acids by suspended bacteria at depth. Chemoautotrophic bacteria utilizing the RubisCO enzyme and Calvin Cycle to reduce inorganic carbon could contribute 13 C-depleted fatty acids to the
interior Canada Basin while their biomass would be isotopically similar to heterotrophic bacteria (Hayes, 2001; Sakata
et al., 2008). The genetic potential for this metabolic pathway has been identified at mesopelagic depths of other oligotrophic regions (Swan et al., 2011), and the expected δ 13 C
value of chemoautotroph-derived fatty acids of ∼ −28 ‰ is
similar to observed δ 13 C values for C16 and C18 between
1000 and 2500 m depth. This value is calculated from a
likely isotopic fractionation between DIC and fatty acids of
∼ 29 ‰ (Sakata et al., 2008) and the δ 13 C value of DIC between 500 and 2500 m which is +1 ‰ (Griffith et al., 2012).
With defined end-member δ 13 C values for bacterial heterotrophs and chemoautotrophs, it is also possible to calculate their proportions through two-component isotopic mixwww.biogeosciences.net/10/7065/2013/
0.15
-25.5
δ13Cbacteria
(δsurface − δadvected )
· fadvected
(1 + fbacteria )
(δmeasured + fbacteria · δsurface )
+
(1 + fbacteria )
δbacteria =
fsurface
0.20
-25.0
-26.5
-27.0
zie Rive
r
70%
Phyto
plankto
n
Co
pep
od
Ice
Be
au
Al
for
ga
tS
e
lop
e
80%
90%
-27.5
-28.0
0.00
0.05
0.10
0.15
% Chemoautrophic Bacteria
Source
100%
0.20
fadvected
Fig. 6. Results of isotopic mass balance model for δ 13 Cbacteria as
a function of fadvected between 1000 and 2500 m depth. Each line
represents a solution for isotopically distinct sources of advected organic carbon with fsurface plotted on the secondary horizontal axis
and the fraction of chemoautotrophic vs. heterotrophic bacteria on
the secondary vertical axis. fbacteria is 0.8.
ing based on model output δbacteria (Fig. 6, secondary vertical axis). Chemoautotrophic production of fatty acids appears to be a significant contributor to the total fatty acid
pool regardless of the advected source of fatty acids. A minimum contribution from chemoautotrophic bacteria of 67 %
is obtained in the unlikely case of purely terrestrial advected
material (δadvected = −35.0 ‰ representing Mackenzie River
POC) with a maximum fadvected value of 0.2. This result suggests that, at minimum, chemoautotrophic bacteria contribute
67 % of the total fatty acids recovered from suspended particulate material.
4.6
Allochthonous fatty acids between 3000 and 3775 m
In the deepest 1000 m, the abundance of total fatty acids
no longer decreases with depth (Fig. 2a), exhibiting a similar trend to prokaryotic abundance (Uchimiya et al., 2013).
Biogeosciences, 10, 7065–7080, 2013
7076
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
The distribution of fatty acids is also distinct from depths
above with a greater representation of long-chain fatty acids
(C20−24 ), BFAs and MUFAs (Fig. 2b). This compositional
difference is likely a reflection of an allochthonous source of
particulate matter to the deep basin. Re-suspension and lateral transport of sediments from surrounding margins dominates sinking POC at these depths (Hwang et al., 2008; Honjo
et al., 2010), and this has also been identified as an important component of suspended POC (Griffith et al., 2012). The
source of this allochthonous organic carbon could be the terrestrially dominated Mackenzie and Beaufort slopes to the
south or the Chukchi slope and base of the Northwind Ridge
to the west. At the base of the Beaufort Slope, shallow sediments host abundant short-chain SFAs and MUFAs, as well
as proportionally important long-chain fatty acids (C23−32 )
and BFAs (Belicka et al., 2004). Further investigations of
long-chain fatty acids at the base of the Beaufort slope revealed a normal distribution of even-numbered SFAs centered around C24 which derive primarily from plant waxes
(Drenzek et al., 2007). Combined, these resemble the distribution of fatty acids in suspended POC (Fig. 2a) with the
exception of the shorter maximum chain length. Although
C24 is the most abundant long-chain fatty acid in suspended
POC, we do not detect C26−32 fatty acids and suspect these
may have been lost to degradation during their suspension in
oxic bottom waters (cf. Rontani et al., 2012). Organic carbon
in the sediments of the Chukchi slope reflects primarily a marine source from the productive Chukchi Sea (Belicka et al.,
2002, 2004). The distribution of fatty acids is subtly different than the base of the Beaufort slope (Belicka et al., 2004)
with only trace C14 saturated fatty acids, and a distribution
of long-chain fatty acids centered around C26 rather than C24
(Belicka et al., 2002). These differences, combined with the
greatest particle load observed in the southern Canada Basin
(Jackson et al., 2010), make the Beaufort slope a more likely
source region for suspended POC in the abyssal Canada
Basin than the Northwind Ridge.
There are also isotopic differences between the deepest
1000 m and above. The δ 13 C value of DOC and suspended
POC are different by ∼ 1.5 ‰, unlike the majority of the water column above (Fig. 4a; Griffith et al., 2012). But, in general, there is a trend towards 13 C-enrichment of SFAs resulting in more isotopic similarity between suspended POC and
SFAs, as well as between SFAs and BFAs at these depths (Table 2; Fig. 4a). It is possible that intense bacterial heterotrophy supported by re-suspended sedimentary organic carbon
contributes a larger proportion of SFAs at deep depths. Another possibility is that a larger proportion of total fatty acids
is delivered to the suspended POC reservoir from a sedimentary source. The isotopic variability in fatty acids from the
deepest depth, 3775 m, may reflect this greater sedimentary
source.
The exceptions to this pattern are C12 and iso-C17 fatty
acids, both of which have δ 13 C values more negative than
any value higher in the water column (Fig. 4a). δ 13 C values
Biogeosciences, 10, 7065–7080, 2013
of C12 and iso-C17 at 3000 m are also more negative than
fatty acids in the Mackenzie River (Goñi et al., 2005). Although some of these values can therefore be explained by a
terrestrial source, a more 13 C-depleted origin is required for
iso-C17 . Bacterial oxidizers of 13 C-depleted methane may be
their origin since methane and gas hydrates have been observed in the coastal Beaufort Sea (Dallimore and Collett,
1995; Paull et al., 2007). Synthesis of iso-C17 could occur
in sediments hosting methane hydrates that are subsequently
mobilized, or iso-C17 could be produced in situ if there is a
source of methane to the deep basin.
5
Conclusions
In the interior Canada Basin, suspended fatty acids show evidence of both advected and in situ sources. Surface waters
host fatty acids that are more depleted in 13 C than in the
dark basin below and also reflect contrasting ecological conditions under ice cover compared to open water. The 13 C
depletion, not observed in DIC or DOC, are likely to result from slowly growing diatoms, but possibly also from the
delivery of terrestrial organic carbon to the central Canada
Basin. Deeper depths appear to be isolated from the effects
of ice cover, but at all depths, a strong isotopic similarity between POC and branched fatty acids is apparent supporting
the hypothesis that intense bacterial heterotrophy contributes
to a weak biological pump in the Canada Basin (Honjo et
al., 2010). An additional, 13 C-depleted source of saturated,
even-numbered fatty acids between 1000 and 2500 m is also
indicated, dominantly (> 67 %) of chemoautotrophic origin.
Lateral advection of DOC from the Chukchi Sea, and POC
re-suspended from sediments are also potential sources. We
believe that the excess abundance of prokaryotes in the deep
Canada Basin, compared to sinking POC flux (Nagata et al.,
2010; Uchimiya et al., 2013; Yokokawa et al., 2013), could
therefore be explained by a combination of bacterial heterotrophs supported by a lateral supply of organic carbon
and chemoautrotrophic bacteria utilizing the Calvin Cycle to
fix inorganic carbon with a yet unknown energy metabolism.
Fatty acids in the deepest 1000 m reflect the contributions
of re-suspended sediments (Hwang et al., 2008) with greater
relative abundances of long-chain fatty acids (C20−24 ), and
isotopic dissimilarity compared to shallower depths. Two individual fatty acids recovered from 3000 m and below, C12
and iso-C17 are too depleted in 13 C to derive from the water
column or shallow sediments and more likely are produced
by methane oxidizing bacteria hinting at a poorly defined
methane cycle in the abyssal Canada Basin.
Supplementary material related to this article is
available online at http://www.biogeosciences.net/10/
7065/2013/bg-10-7065-2013-supplement.pdf.
www.biogeosciences.net/10/7065/2013/
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
Acknowledgements. We are grateful to K. Brown, W. Burt,
M. Dempsey, R. Krishfield, S. Manganini, A. Proshutinsky,
S. Zimmerman and the captain and crew of the CCGS L. S. St Laurent, as well as X. Philippon and C. Johnson for their analytical
assistance. This manuscript has been improved by discussions with
B. Van Mooy. The WHOI Postdoctoral Scholar Program and NSF
Cooperative Agreement for the Operation of a National Ocean
Sciences Accelerator Mass Spectrometry Facility (OCE-0753487)
supported S. R. Shah and the WHOI Arctic Research Initiative
funded compound-specific isotopic analysis. The 2008 JOIS
hydrographic program was supported by Fisheries and Oceans
Canada, the Canadian International Polar Year Office, and the
US National Science Foundation (OPP-0424864; lead-PI Andrey
Proshutinsky).
Edited by: N. Ohkouchi
References
Balkwill, D. L., Leach, F. R., Wilson, J. T., McNabb, J. F., and
White, D. C.: Equivalence of Microbial Biomass Measures
Based on Membrane Lipid and Cell Wall Components, Adenosine Triphosphate, and Direct Counts in Subsurface Aquifer Sediments, Microb. Ecol., 16, 73–84, 1988.
Belicka, L. L., Macdonald, R. W., and Harvey, H. R.: Sources and
transport of organic carbon to shelf, slope, and basin surface sediments of the Arctic Ocean, Deep-Sea Res. Pt. I, 49, 1463–1483,
2002.
Belicka, L. L., Macdonald, R. W., Yunker, M. B., and Harvey,
H. R.: The role of depositional regime on carbon transport and
preservation in Arctic Ocean sediments, Mar. Chem., 86, 65–88,
doi:10.1016/j.marchem.2003.12.006, 2004.
Belt, S. T., Massé, G., Vare, L. L., Rowland, S. J., Poulin, M.,
Sicre, M.-A., Sampei, M., and Fortier, L.: Distinctive 13C isotopic signature distinguishes a novel sea ice biomarker in Arctic sediments and sediment traps, Mar. Chem., 112, 158–167,
doi:10.1016/j.marchem.2008.09.002, 2008.
Blair, N. E., Leu, A., Muñoz, E., Olsen, J., Kwong, E., and Des
Marais, D. J.: Carbon isotopic fractionation in heterotrophic
microbial metabolism, Appl. Environ. Microb., 50, 996–1001,
1985.
Boschker, H. T. S., Kromkamp, J. C., and Middelburg, J. J.:
Biomarker and carbon isotopic constraints on bacterial and algal
community structure and functioning in a turbid, tidal estuary,
Limnol. Oceanogr., 50, 70–80, 2005.
Budge, S. M., Wooller, M. J., Springer, A. M., Iverson, S. J.,
McRoy, C. P., and Divoky, G. J.: Tracing carbon flow in an arctic
marine food web using fatty acid-stable isotope analysis, Oecologia, 157, 117–29, doi:10.1007/s00442-008-1053-7, 2008.
Burd, A. B. and Jackson, G. A.: Particle Aggregation,
Annu.
Rev.
Mari.
Sci.,
1,
65–90,
doi:10.1146/annurev.marine.010908.163904, 2009.
Cai, W.-J., Chen, L., Chen, B., Gao, Z., Lee, S. H., Chen, J., Pierrot, D., Sullivan, K., Wang, Y., Hu, X., Huang, W.-J., Zhang, Y.,
Xu, S., Murata, A., Grebmeier, J. M., Jones, E. P., and Zhang, H.:
Decrease in the CO2 uptake capacity in an ice-free Arctic Ocean
basin, Science, 329, 556–559, doi:10.1126/science.1189338,
2010.
www.biogeosciences.net/10/7065/2013/
7077
Christian, J. R. and Karl, D. M.: Microbial community structure at
the US-Joint Global Ocean flux Study Station ALOHA: Inverse
methods for estimating biochemical indicator ratios, J. Geophys.
Res., 99, 14269–14276, 1994.
Connelly, T. L., Deibel, D., and Parrish, C. C.: Biogeochemistry
of near-bottom suspended particulate matter of the Beaufort Sea
shelf (Arctic Ocean): C, N, P, δ13C and fatty acids, Cont. Shelf
Res., 43, 120–132, doi:10.1016/j.csr.2012.05.011, 2012.
Dallimore, S. R. and Collett, T. S.: Intrapermafrost gas hydrates
from a deep core hole in the Mackenzie Delta, Northwest
Territories, Canada, Geology, 23, 527–530, doi:10.1130/00917613(1995)023<0527:IGHFAD>2.3.CO;2, 1995.
Davis, J. and Benner, R.: Seasonal trends in the abundance,
composition and bioavailability of particulate and dissolved
organic matter in the Chukchi/Beaufort Seas and western Canada Basin, Deep-Sea Res. Pt. II, 52, 3396–3410,
doi:10.1016/j.dsr2.2005.09.006, 2005.
Davis, J. and Benner, R.: Quantitative estimates of labile and semilabile dissolved organic carbon in the western Arctic Ocean:
A molecular approach, Limnol. Oceanogr., 52, 2434–2444,
doi:10.4319/lo.2007.52.6.2434, 2007.
Drenzek, N. J., Montlucon, D. B., Yunker, M. B., Macdonald, R.
W., and Eglinton, T. I.: Constraints on the origin of sedimentary organic carbon in the Beaufort Sea from coupled molecular 13C and 14C measurements, Mar. Chem., 103, 146–162,
doi:10.1016/j.marchem.2006.06.017, 2007.
Engel, A., Thoms, S., Riebesell, U., Rochelle-Newall, E., and
Zondervan, I.: Polysaccharide aggregation as a potential sink
of marine dissolved organic carbon, Nature, 428, 27–30,
doi:10.1038/nature02453, 2004.
Findlay, R. H., King, G. M., and Watling, L.: Efficacy of Phospholipid Analysis in Determining Microbial Biomass in Sediments,
Appl. Environ. Microb., 55, 2888–2893, 1989.
Forest, A., Sampei, M., Hattori, H., Makabe, R., Sasaki, H.,
Fukuchi, M., Wassmann, P., and Fortier, L.: Particulate organic
carbon fluxes on the slope of the Mackenzie Shelf (Beaufort Sea):
Physical and biological forcing of shelf-basin exchanges, J. Marine Syst., 68, 39–54, doi:10.1016/j.jmarsys.2006.10.008, 2007.
Gardner, W. D., Richardson, M. J., Carlson, C. A., Hansell, D. A.,
and Mishonov, A. V: Determining true particulate organic carbon: bottles, pumps and methodologies, Deep-Sea Res. Pt. II,
50, 655–674, doi:10.1016/S0967-0645(02)00589-1, 2003.
Goñi, M. A., Yunker, M. B., Macdonald, R. W., and Eglinton, T. I.: The supply and preservation of ancient and modern components of organic carbon in the Canadian Beaufort Shelf of the Arctic Ocean, Mar. Chem., 93, 53–73,
doi:10.1016/j.marchem.2004.08.001, 2005.
Gosselin, M., Levasseur, M., Wheeler, Patricia, A., Horner, R. A.,
and Booth, B. C.: New measurements of phytoplankton and ice
algal production in the Arctic Ocean, Deep-Sea Res. Pt. II, 44,
1623–1644, 1998.
Grebmeier, J. M., Moore, S. E., and Overland, J. E.: Biological response to recent Pacific Arctic sea ice retreats, Eos, Transactions
American Geophysical Union, 91, 2008–2010, 2010.
Griffith, D. R., McNichol, A. P., Xu, L., McLaughlin, F. A., Macdonald, R. W., Brown, K. A., and Eglinton, T. I.: Carbon dynamics in the western Arctic Ocean: insights from full-depth carbon isotope profiles of DIC, DOC, and POC, Biogeosciences, 9,
1217–1224, doi:10.5194/bg-9-1217-2012, 2012.
Biogeosciences, 10, 7065–7080, 2013
7078
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
Guay, C. K. H., McLaughlin, F. A., and Yamamoto-Kawai, M.:
Differentiating fluvial components of upper Canada Basin waters on the basis of measurements of dissolved barium combined
with other physical and chemical tracers, J. Geophys. Res., 114,
C00A09, doi:10.1029/2008JC005099, 2009.
Gundersen, K., Heldal, M., Norland, S., Purdie, D. A., and Knap,
A. H.: Elemental C, N, and P cell content of individual bacteria collected at the Bermuda Atlantic Time-Series Study (BATS)
site, Limnol. Oceanogr., 47, 1525–1530, 2002.
Gutiérrez, M. H., Pantoja, S., and Lange, C. B.: Biogeochemical
significance of fatty acid distribution in the coastal upwelling
ecosystem off Concepción (36◦ S), Chile, Org. Geochem., 49,
56–67, doi:10.1016/j.orggeochem.2012.05.010, 2012.
Hamanaka, J., Tanoue, E., Hama, T., and Handa, N.: Production
and export of particulate fatty acids, carbohydrates and combined amino acids in the euphotic zone, Mar. Chem., 77, 55–69,
doi:10.1016/S0304-4203(01)00075-5, 2002.
Hansell, D. A., Kadko, D., and Bates, N. R.: Degradation of terrigenous dissolved organic carbon in the western Arctic Ocean,
Science, 304, 858–861, doi:10.1126/science.1096175, 2004.
Hayes, J. M.: Fractionation of the Isotopes of Carbon and Hydrogen in Biosynthetic Processes, in Reviews, in: Mineralogy and
Geochemistry, vol. 43, edited by: Valley, J. W. and Cole, D. R.,
225–278, Mineralogical Society of America, Washington, D.C.,
2001.
He, J., Zhang, F., Lin, L., Ma, Y., and Chen, J.: Bacterioplankton
and picophytoplankton abundance, biomass, and distribution in
the Western Canada Basin during summer 2008, Deep-Sea Res.
Pt. II, 81–84, 36–45, doi:10.1016/j.dsr2.2012.08.018, 2012.
Herndl, G. J., Reinthaler, T., Teira, E., van Aken, H., Veth, C.,
Pernthaler, A., and Pernthaler, J.: Contribution of Archaea to
total prokaryotic production in the deep Atlantic Ocean, Appl.
Environ. Microb., 71, 2303–2309, doi:10.1128/AEM.71.5.23032309.2005, 2005.
Honjo, S., Krishfield, R. A., Eglinton, T. I., Manganini, S. J., Kemp,
J. N., Doherty, K., Hwang, J., McKee, T. K., and Takizawa, T.:
Biological pump processes in the cryopelagic and hemipelagic
Arctic Ocean: Canada Basin and Chukchi Rise, Prog. Oceanogr.,
85, 137–170, doi:10.1016/j.pocean.2010.02.009, 2010.
Hwang, J., Eglinton, T. I., Krishfield, R. A., Manganini,
S. J., and Honjo, S.: Lateral organic carbon supply to
the deep Canada Basin, Geophys. Res. Lett., 35, L11607,
doi:10.1029/2008GL034271, 2008.
Jackson, J. M., Allen, S. E., Carmack, E. C., and McLaughlin, F. A.:
Suspended particles in the Canada Basin from optical and bottle
data, 2003–2008, Ocean Sci., 6, 799–813, doi:10.5194/os-6-7992010, 2010.
Kaneda, T.: Iso- and anteiso-fatty acids in bacteria: biosynthesis,
function, and taxonomic significance, Microbiol. Rev., 55, 288–
302, 1991.
Karner, M. B., DeLong, E. F., and Karl, D. M.: Archaeal dominance
in the mesopelagic zone of the Pacific Ocean, Nature, 409, 507–
510, doi:10.1038/35054051, 2001.
Kirchman, D. L., Elifantz, H., Dittel, A. I., Malmstrom, R. R., and
Cottrell, M. T.: Standing stocks and activity of Archaea and Bacteria in the western Arctic Ocean, Limnol. Oceanogr., 52, 495–
507, 2007.
Biogeosciences, 10, 7065–7080, 2013
Lee, S. H., Kang, Y.-C., and Fuhrman, J. A.: Imperfect retention of
natural bacterioplankton cells by glass fiber filters, Mar. Ecol.Prog. Ser., 119, 285–290, 1995.
Lee, S. H., Joo, H. M., Liu, Z., Chen, J., and He, J.: Phytoplankton productivity in newly opened waters of the Western Arctic Ocean, Deep-Sea Res. Pt. II, 81–84, 18–27,
doi:10.1016/j.dsr2.2011.06.005, 2012.
Li, W. K. W., McLaughlin, F. A., Lovejoy, C., and Carmack, E. C.:
Smallest algae thrive as the Arctic Ocean freshens, Science, 326,
539, doi:10.1126/science.1179798, 2009.
Loh, A. N., Canuel, E. A., and Bauer, J. E.: Potential source and diagenetic signatures of oceanic dissolved and particulate organic
matter as distinguished by lipid biomarker distributions, Mar.
Chem., 112, 189–202, doi:10.1016/j.marchem.2008.08.005,
2008.
Macdonald, R. W., McLaughlin, F. A., and Carmack, E. C.: Fresh
water and its sources during the SHEBA drift in the Canada
Basin of the Arctic Ocean, Deep-Sea Res. Pt. I, 49, 1769–1785,
doi:10.1016/S0967-0637(02)00097-3, 2002.
Martin, J., Tremblay, J. É., and Price, N. M.: Nutritive and photosynthetic ecology of subsurface chlorophyll maxima in Canadian
Arctic waters, Biogeosciences, 9, 5353–5371, doi:10.5194/bg-95353-2012, 2012.
Maslanik, J., Stroeve, J., Fowler, C., and Emery, W.: Distribution
and trends in Arctic sea ice age through spring 2011, Geophys.
Res. Lett., 38, 2–7, doi:10.1029/2011GL047735, 2011.
Mathis, J. T., Pickart, R. S., Hansell, D. A., Kadko, D., and
Bates, N. R.: Eddy transport of organic carbon and nutrients from the Chukchi Shelf: Impact on the upper halocline
of the western Arctic Ocean, J. Geophys. Res., 112, C05011,
doi:10.1029/2006JC003899, 2007.
Mayzaud, P., Boutoute, M., and Gasparini, S.: Differential response
of fatty acid composition in the different lipid classes from particulate matter in a high arctic fjord (Kongsfjorden, Svalbard), Mar.
Chem., 151, 23–34, doi:10.1016/j.marchem.2013.02.009, 2013.
McLaughlin, F. A. and Carmack, E. C.: Deepening of the
nutricline and chlorophyll maximum in the Canada Basin
interior, 2003–2009, Geophys. Res. Lett., 37, L24602,
doi:10.1029/2010GL045459, 2010.
McLaughlin, F. A., Carmack, E. C., Proshutinsky, A., Krishfield,
R. A., Guay, C., Yamamoto-Kawai, M., Jackson, J. M., and
Williams, B.: The rapid response of the Canada Basin to climate forcing: From bellweather to alarm bells, Oceanography,
24, 146–159, 2011.
McPhee, M. G., Proshutinsky, A., Morison, J. H., Steele,
M., and Alkire, M. B.: Rapid change in freshwater content of the Arctic Ocean, Geophys. Res. Lett., 36, L10602,
doi:10.1029/2009GL037525, 2009.
Monson, K. D. and Hayes, J. M.: Carbon isotopic fractionation in
the biosynthesis of bacterial fatty acids. Ozonolysis of unsaturated fatty acids as a means of determining the intramolecular
distribution of carbon isotopes, Geochim. Cosmochim. Ac., 46,
139–149, 1982.
Moran, S. B., Charette, M. A., Pike, S. M., and Wicklund, C. A.:
Differences in seawater particulate organic carbon concentration
in samples collected using small- and large-volume methods: the
importance of DOC adsorption to the filter blank, Mar. Chem.,
67, 33–42, doi:10.1016/S0304-4203(99)00047-X, 1999.
www.biogeosciences.net/10/7065/2013/
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
Moran, S. B., Kelly, R. P., Hagstrom, K., Smith, J. N., Grebmeier, J.
M., Cooper, L. W., Cota, G. F., Walsh, J. J., Bates, N. R., Hansell,
D. A., Maslowski, W., Nelson, R. P., and Mulsow, S.: Seasonal
changes in POC export flux in the Chukchi Sea and implications for water column-benthic coupling in Arctic shelves, DeepSea Res. Pt. II, 52, 3427–3451, doi:10.1016/j.dsr2.2005.09.011,
2005.
Nagata, T., Tamburini, C., Arístegui, J., Baltar, F., Bochdansky,
A. B., Fonda-Umani, S., Fukuda, H., Gogou, A., Hansell,
D. A., Hansman, R. L., Herndl, G. J., Panagiotopoulous, C.,
Reinthaler, T., Sohrin, R., Verdugo, P., Yamada, N., Yamashita,
Y., Yokokawa, T., and Bartlett, D. H.: Emerging concepts on microbial processes in the bathypelagic ocean – ecology, biogeochemistry, and genomics, Deep-Sea Res. Pt. II, 57, 1519–1536,
doi:10.1016/j.dsr2.2010.02.019, 2010.
Naidu, A. S., Cooper, L. W., Finney, B. P., Macdonald, R. W.,
Alexander, C., and Semiletov, I. P.: Organic carbon isotope ratios
(δ13C) of Arctic Amerasian Continental shelf sediments, Int. J.
Earth Sci., 89, 522–532, doi:10.1007/s005310000121, 2000.
O’Brien, M. C., Melling, H., Pedersen, T. F., and Macdonald,
R. W.: The role of eddies on particle flux in the Canada
Basin of the Arctic Ocean, Deep-Sea Res. Pt. I, 71, 1–20,
doi:10.1016/j.dsr.2012.10.004, 2013.
Oliver, J. D. and Colwell, R. R.: Extractable lipids of gram-negative
marine bacteria: phospholipid composition., J. Bacteriol., 114,
897–908, 1973.
Oliver, J. D. and Stringer, W. F.: Lipid Composition of a Psychrophilic Marine Vibrio sp. During Starvation-Induced Morphogenesis, Appl. Environ. Microb., 47, 461–466, 1984.
Ortega-Retuerta, E., Jeffrey, W. H., Babin, M., Bélanger, S., Benner, R., Marie, D., Matsuoka, A., Raimbault, P., and Joux, F.:
Carbon fluxes in the Canadian Arctic: patterns and drivers of bacterial abundance, production and respiration on the Beaufort Sea
margin, Biogeosciences, 9, 3679–3692, doi:10.5194/bg-9-36792012, 2012.
Paull, C. K., Ussler, W. I., Dallimore, S. R., Blasco, S. M.,
Lorenson, T. D., Melling, H., Medioli, B. E., Nixon, F. M.,
and McLaughlin, F. A.: Origin of pingo-like features on the
Beaufort Sea shelf and their possible relationship to decomposing methane gas hydrates, Geophys. Res. Lett., 34, 1–5,
doi:10.1029/2006GL027977, 2007.
Pickart, R. S.: Shelfbreak circulation in the Alaskan Beaufort Sea:
Mean structure and variability, J. Geophys. Res., 109, 1–14,
doi:10.1029/2003JC001912, 2004.
Popp, B. N., Laws, E. A., Bidigare, R. R., Dore, J. E., Hanson, K.
L., and Wakeham, S. G.: Effect of phytoplankton cell geometry
on carbon isotopic fractionation, Geochim. Cosmochim. Ac., 62,
69–77, 1998.
Rich, J., Gosselin, M., Sherr, E. B., Sherr, B. F., and Kirchman,
D. L.: High bacterial production, uptake and concentrations of
dissolved organic matter in the Central Arctic Ocean, Deep-Sea
Res. Pt. II, 44, 1645–1663, 1998.
Rontani, J.-F., Charriere, B., Petit, M., Vaultier, F., Heipieper,
H. J., Link, H., Chaillou, G., and Sempéré, R.: Degradation
state of organic matter in surface sediments from the Southern
Beaufort Sea: a lipid approach, Biogeosciences, 9, 3513–3530,
doi:10.5194/bg-9-3513-2012, 2012.
Sakata, S., Hayes, J. M., Rohmer, M., Hooper, A. B.,
and Seemann, M.: Stable carbon-isotopic compositions of
www.biogeosciences.net/10/7065/2013/
7079
lipids isolated from the ammonia-oxidizing chemoautotroph
Nitrosomonas europaea, Org. Geochem., 39, 1725–1734,
doi:10.1016/j.orggeochem.2008.08.005, 2008.
Schouten, S., Klein Breteler, W. C., Blokker, P., Schogt, N., Rijpstra, W. I. C., Grice, K., Baas, M., and Sinninghe Damsté, J. S.:
Biosynthetic effects on the stable carbon isotopic compositions
of algal lipids: implications for deciphering the carbon isotopic
biomarker record, Geochim. Cosmochim. Ac., 62, 1397–1406,
doi:10.1016/S0016-7037(98)00076-3, 1998.
Schultz, D. M. and Quinn, J. G.: Fatty Acids in Surface Particulate
Matter From the North Atlantic, J. Fish. Res. Board Can., 29,
1482–1486, 1972.
Schultz, D. M. and Quinn, J. G.: Fatty acid composition of organic
detritus from Spartina alterniflora, Estuar. Coast. Mar. Sci., 1,
177–190, doi:10.1016/0302-3524(73)90068-6, 1973.
Shen, Y., Fichot, C. G., and Benner, R.: Dissolved organic matter composition and bioavailability reflect ecosystem productivity in the Western Arctic Ocean, Biogeosciences, 9, 4993–5005,
doi:10.5194/bg-9-4993-2012, 2012.
Sherr, B. F. and Sherr, E. B.: Community respiration/production and
bacterial activity in the upper water column of the central Arctic
Ocean, Deep-Sea Res. Pt. I, 50, 529–542, doi:10.1016/S09670637(03)00030-X, 2003.
Sherr, E. B., Sherr, B. F., Wheeler, P. A., and Thompson,
K.: Temporal and spatial variation in stocks of autotrophic
and heterotrophic microbes in the upper water column of
the central Arctic Ocean, Deep-Sea Res. Pt. I, 50, 557–571,
doi:10.1016/S0967-0637(03)00031-1, 2003.
Stroeve, J., Holland, M. M., Meier, W., Scambos, T., and Serreze,
M.: Arctic sea ice decline: Faster than forecast, Geophys. Res.
Lett., 34, L09501, doi:10.1029/2007GL029703, 2007.
Swan, B. K., Martinez-Garcia, M., Preston, C. M., Sczyrba, A.,
Woyke, T., Lamy, D., Reinthaler, T., Poulton, N. J., Dashiell, E.,
Masland, P., Lluesma Gomez, M., Sieracki, M. E., DeLong, E. F.,
Herndl, G. J., and Stepanauskas, R.: Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark
Ocean, Science, 333, 1296–1299, doi:10.1126/science.1203690,
2011.
Tolosa, I., Vescovali, I., LeBlond, N., Marty, J.-C., de Mora, S.,
and Prieur, L.: Distribution of pigments and fatty acid biomarkers in particulate matter from the frontal structure of the Alboran Sea (SW Mediterranean Sea), Mar. Chem., 88, 103–125,
doi:10.1016/j.marchem.2004.03.005, 2004.
Tolosa, I., Fiorini, S., Gasser, B., Martín, J., and Miquel, J. C.: Carbon sources in suspended particles and surface sediments from
the Beaufort Sea revealed by molecular lipid biomarkers and
compound-specific isotope analysis, Biogeosciences, 10, 2061–
2087, doi:10.5194/bg-10-2061-2013, 2013.
Uchimiya, M., Fukuda, H., Nishino, S., Kikuchi, T., Ogawa, H.,
and Nagata, T.: Vertical distribution of prokaryote production
and abundance in the mesopelagic and bathypelagic layers of the
Canada Basin, western Arctic: Implications for the mode and extent of organic carbon delivery, Deep-Sea Res. Pt. I, 71, 103–112,
doi:10.1016/j.dsr.2012.10.001, 2013.
Wakeham, S. G.: Lipid biomarkers for heterotrophic alteration of
suspended particulate organic matter in oxygenated and anoxic
water columns of the ocean, Deep-Sea Res. Pt. I, 42, 1749–1771,
1995.
Biogeosciences, 10, 7065–7080, 2013
7080
S. R. Shah et al.: Prominent bacterial heterotrophy and sources of 13 C-depleted fatty acids
Wakeham, S. G., Amann, R., Freeman, K. H., Hopmans, E. C., Jørgensen, B. B., Putnam, I. F., Schouten, S., Sinninghe Damsté,
J. S., Talbot, H. M., and Woebken, D.: Microbial ecology of
the stratified water column of the Black Sea as revealed by a
comprehensive biomarker study, Org. Geochem., 38, 2070–2097,
doi:10.1016/j.orggeochem.2007.08.003, 2007.
Wakeham, S. G., Turich, C., Taylor, G. T., Podlaska, A., Scranton, M. I., Li, X. N., Varela, R., and Astor, Y.: Mid-chain
methoxylated fatty acids within the chemocline of the Cariaco
Basin: A chemoautotrophic source?, Org. Geochem., 41, 498–
512, doi:10.1016/j.orggeochem.2010.01.005, 2010.
Walsh, J. J., McRoy, C. P., Coachman, L. K., Georing, J. J., Nihoul,
J. J., Whitledge, T. E., Blackburn, T. H., Parker, P. L., Wirick,
C. D., Shuert, P. G., Grebmeier, J. M., Springer, A. M., Tripp,
R. D., Hansell, D. A., Djenidi, S., Deleersnijder, E., Henriksen,
K., Lund, B. A., Andersen, P., Muller-Karger, F. E., and Dean,
K.: Carbon and nitrogen cycling within the Bering/Chukchi Seas:
source regions for organic matter affecting AOU demands of the
Arctic Ocean, Prog. Oceanogr., 22, 277–359, 1989.
White, D. C., Davis, W. M., Nickels, J. S., King, J. D., and Bobbie,
R. J.: Determination of the Sedimentary Microbial Biomass by
Extractible Lipid Phosphate, Oecologia, 40, 51–62, 1979.
Xu, Y. and Jaffé, R.: Lipid biomarkers in suspended particles from
a subtropical estuary: assessment of seasonal changes in sources
and transport of organic matter, Mar. Environ. Res., 64, 666–678,
doi:10.1016/j.marenvres.2007.07.004, 2007.
Biogeosciences, 10, 7065–7080, 2013
Yamamoto-Kawai, M., McLaughlin, F. A., Carmack, E. C., Nishino,
S., Shimada, K., and Kurita, N.: Surface freshening of the Canada
Basin, 2003–2007: River runoff versus sea ice meltwater, J. Geophys. Res., 114, C00A05, doi:10.1029/2008JC005000, 2009.
Yokokawa, T., Yang, Y., Motegi, C., and Nagata, T.: Largescale geographical variation in prokaryotic abundance and production in meso- and bathypelagic zones of the central Pacific and Southern Ocean, Limnol. Oceanogr., 58, 61–73,
doi:10.4319/lo.2013.58.1.0061, 2013.
Yunker, M. B., Belicka, L. L., Harvey, H. R., and Macdonald, R.
W.: Tracing the inputs and fate of marine and terrigenous organic matter in Arctic Ocean sediments: A multivariate analysis of lipid biomarkers, Deep-Sea Res. Pt. II, 52, 3478–3508,
doi:10.1016/j.dsr2.2005.09.008, 2005.
Zou, L., Sun, M.-Y., and Guo, L.: Temporal variations of organic
carbon inputs into the upper Yukon River: Evidence from fatty
acids and their stable carbon isotopic compositions in dissolved,
colloidal and particulate phases, Org. Geochem., 37, 944–956,
doi:10.1016/j.orggeochem.2006.04.002, 2006.
www.biogeosciences.net/10/7065/2013/